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The microRNA toolkit of insects

View Article: PubMed Central - PubMed

ABSTRACT

Is there a correlation between miRNA diversity and levels of organismic complexity? Exhibiting extraordinary levels of morphological and developmental complexity, insects are the most diverse animal class on earth. Their evolutionary success was in particular shaped by the innovation of holometabolan metamorphosis in endopterygotes. Previously, miRNA evolution had been linked to morphological complexity, but astonishing variation in the currently available miRNA complements of insects made this link unclear. To address this issue, we sequenced the miRNA complement of the hemimetabolan Blattella germanica and reannotated that of two other hemimetabolan species, Locusta migratoria and Acyrthosiphon pisum, and of four holometabolan species, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. Our analyses show that the variation of insect miRNAs is an artefact mainly resulting from poor sampling and inaccurate miRNA annotation, and that insects share a conserved microRNA toolkit of 65 families exhibiting very low variation. For example, the evolutionary shift toward a complete metamorphosis was accompanied only by the acquisition of three and the loss of one miRNA families.

No MeSH data available.


miRNA families and miRNA genes found in the seven species of insects studied.Blattella germanica, Locusta migratoria, Acyrtosiphon pisum, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. The lineages where the miRNA families originated is indicated. miRNAs highlighted in bright green are those identified in the present study for the first time. Those in light green are miRNAs added to a previously known family. Orange colour highlights a miRNA gene found in the genome but without expression data. The origin of the miRNA families indicated in violet was updated.
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f4: miRNA families and miRNA genes found in the seven species of insects studied.Blattella germanica, Locusta migratoria, Acyrtosiphon pisum, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. The lineages where the miRNA families originated is indicated. miRNAs highlighted in bright green are those identified in the present study for the first time. Those in light green are miRNAs added to a previously known family. Orange colour highlights a miRNA gene found in the genome but without expression data. The origin of the miRNA families indicated in violet was updated.

Mentions: From an evolutionary point of view, L. migratoria is the closest relative to B. germanica, for which 833 miRNAs have been reported13. In order to compare this species with B. germanica, we submitted the miRNAs described by Wang et al.13 to the filtering procedure described herein. Results showed that 532 of the originally described L. migratoria miRNAs fulfilled the filtering criteria. From these, we discarded seven candidates that were identified as miRNA duplicated loci resulting from genome assembly artefacts. We also noticed that seven miRNA families present in B. germanica (MIR-2001, MIR-375, MIR-3049, MIR-3770, MIR-317, MIR-316 and MIR-971) were not recorded in L. migratoria. Blast approaches on the genome assembly and on small RNA-seq reads led to find three of them: MIR-317, MIR-316 and MIR-971, as well as a new Mir-10 gene. In summary, 85 conserved miRNA belonging to 57 families were identified in L. migratoria, including a MIR-bg5 gene (Fig. 4). The 444 remaining candidate genes are L. migratoria specific, which gave 365 different mature miRNAs (as some genes expressed identical mature miRNAs) that were grouped into 312 families. Supplementary Data S3 shows the complete reports of these L. migratoria miRNAs, and Supplementary Table S6 shows the correspondence between these miRNAs, the family assigned by us and the miRNA identifiers of Wang et al.13. L. migratoria specific miRNAs are clearly less expressed than conserved miRNAs, as occurs in B. germanica (Fig. 5).


The microRNA toolkit of insects
miRNA families and miRNA genes found in the seven species of insects studied.Blattella germanica, Locusta migratoria, Acyrtosiphon pisum, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. The lineages where the miRNA families originated is indicated. miRNAs highlighted in bright green are those identified in the present study for the first time. Those in light green are miRNAs added to a previously known family. Orange colour highlights a miRNA gene found in the genome but without expression data. The origin of the miRNA families indicated in violet was updated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5121899&req=5

f4: miRNA families and miRNA genes found in the seven species of insects studied.Blattella germanica, Locusta migratoria, Acyrtosiphon pisum, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. The lineages where the miRNA families originated is indicated. miRNAs highlighted in bright green are those identified in the present study for the first time. Those in light green are miRNAs added to a previously known family. Orange colour highlights a miRNA gene found in the genome but without expression data. The origin of the miRNA families indicated in violet was updated.
Mentions: From an evolutionary point of view, L. migratoria is the closest relative to B. germanica, for which 833 miRNAs have been reported13. In order to compare this species with B. germanica, we submitted the miRNAs described by Wang et al.13 to the filtering procedure described herein. Results showed that 532 of the originally described L. migratoria miRNAs fulfilled the filtering criteria. From these, we discarded seven candidates that were identified as miRNA duplicated loci resulting from genome assembly artefacts. We also noticed that seven miRNA families present in B. germanica (MIR-2001, MIR-375, MIR-3049, MIR-3770, MIR-317, MIR-316 and MIR-971) were not recorded in L. migratoria. Blast approaches on the genome assembly and on small RNA-seq reads led to find three of them: MIR-317, MIR-316 and MIR-971, as well as a new Mir-10 gene. In summary, 85 conserved miRNA belonging to 57 families were identified in L. migratoria, including a MIR-bg5 gene (Fig. 4). The 444 remaining candidate genes are L. migratoria specific, which gave 365 different mature miRNAs (as some genes expressed identical mature miRNAs) that were grouped into 312 families. Supplementary Data S3 shows the complete reports of these L. migratoria miRNAs, and Supplementary Table S6 shows the correspondence between these miRNAs, the family assigned by us and the miRNA identifiers of Wang et al.13. L. migratoria specific miRNAs are clearly less expressed than conserved miRNAs, as occurs in B. germanica (Fig. 5).

View Article: PubMed Central - PubMed

ABSTRACT

Is there a correlation between miRNA diversity and levels of organismic complexity? Exhibiting extraordinary levels of morphological and developmental complexity, insects are the most diverse animal class on earth. Their evolutionary success was in particular shaped by the innovation of holometabolan metamorphosis in endopterygotes. Previously, miRNA evolution had been linked to morphological complexity, but astonishing variation in the currently available miRNA complements of insects made this link unclear. To address this issue, we sequenced the miRNA complement of the hemimetabolan Blattella germanica and reannotated that of two other hemimetabolan species, Locusta migratoria and Acyrthosiphon pisum, and of four holometabolan species, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. Our analyses show that the variation of insect miRNAs is an artefact mainly resulting from poor sampling and inaccurate miRNA annotation, and that insects share a conserved microRNA toolkit of 65 families exhibiting very low variation. For example, the evolutionary shift toward a complete metamorphosis was accompanied only by the acquisition of three and the loss of one miRNA families.

No MeSH data available.